Coccidiosis of the wild rabbit \(Oryctolagus cuniculus\) in

Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2003101p51
COCCIDIOSIS OF THE WILD RABBIT
G R È S V.*,
VOZA
(ORYCTOLAGUS CUNICULUS)
IN FRANCE
T . * . C H A B A U D A.* & L A N D A U I.*
Summary :
Résumé
In 1998-1999 a survey of coccidiosis in wild rabbits was carried
out in six different localities in France. About five individuals were
caught monthly in each locality and a total of 2 5 4 wild rabbits
was examined. Ten species of Coccidia were identified: Eimeria
perforans, E. flavescens, E. piriformis, E. exigua, E. media,
E. magna, E. coecicola, E. stiedai, E. roobroucki, E. inteslinalis.
Intensity of infection in young individuals was higher than in
adults. Intensity was highest in winter but, as there are no young
rabbits in winter, in young individuals it was higher in spring and
autumn than in summer. Intensities were higher in the northern
rather than in southern localities. Ranking of prevalence was
remarkably stable, in contrast to the variability of the parasitic
load. The equilibrium between congeneric species of rabbit
coccidia (stable prevalence rank, variable parasitic load) is
thought to be probably the consequence of the opportunistic
feeding habits of rabbits
K E Y W O R D S : Eimeria, wild rabbit, congeneric species.
: LA COCCIDIOSE DU LAPIN DE GARENNE (ORYCTOLAGUS
CUNICULUS) EN FRANCE
En 1998-1999, nous avons mené une étude sur la coccidiose du
lapin de garenne dans six localités différentes en France. Pour
chaque site, cinq individus environ ont été capturés mensuellement
et un total de 254 lapins a été examiné. Dix espèces de
Coccidies ont pu être identifiées : Eimeria perforans,
E. flavescens, E. piriformis, E. exigua, E. media, E. magna ,
E. coecicola, E. stiedai, E. roobroucki, E. intestinalis. Chez les
jeunes lapins, l'intensité de l'infection apparaît plus élevée que
chez les adultes. C'est en hiver que l'intensité de l'infection des
adultes est la plus élevée. Par contre, chez les juvéniles, qui
n'apparaissent qu'au printemps, l'infection est plus importante au
printemps et à l'automne qu'en été. Les sites du nord présentent les
intensités les plus élevées. L'ordre des prévalences apparaît
remarquablement stable comparé à la variabilité de la charge
parasitaire. L'équilibre entre les espèces congénériques de
coccidies de lapins (ordre des prévalences stable, charge
parasitaire variable) pourrait être la conséquence du comportement
alimentaire opportuniste du lapin de garenne.
MOTS CLÉS : Eimeria, lapin de garenne, espèces congénériques.
INTRODUCTION
R
MATERIALS AND METHODS
a b b i t Eimeria
h a v e b e e n e x t e n s i v e l y u s e d as
experimental
models,
b e c a u s e o f the
S T U D Y AREAS
small
size o f their host, its great fecundity a n d e c o -
T h e survey w a s carried out in six study areas.
this g r o u p o f
Arjuzanx reserve c o v e r s 2,452 ha in the south-west o f
parasites is e x c e p t i o n a l l y e x t e n s i v e a n d precise ( C o u -
France (department o f Landes, 4 4 ° 0 0 ' N, 0° 5 1 ' W ) . T h e
dert et al., 1 9 9 5 ) , but it mainly c o n c e r n s the d o m e s t i c
climate is oceanic, the mean annual rainfall is 1,016 mm
nomic
importance.
Information
on
rabbit. T h e p r e s e n t w o r k is an attempt to c o m p a r e
and
the fauna o f wild and d o m e s t i c rabbits and to unders-
w e r e caught in mesophilic land colonised by Ilex
euro-
tand the type o f b a l a n c e a c h i e v e d b e t w e e n the para-
peus,
sco-
site s p e c i e s . Results w e r e
paria.
compared
with
reports
the m e a n
Caluna
annual
vulgaris,
temperature
Erica
cinerea
12.9° C. Rabbits
and Erica
from t h e few o t h e r c o u n t r i e s w e r e similar surveys
Chèvreloup arboretum o c c u p i e s 2 0 0 ha in Versailles
were
near Paris (department o f Yvelines, 48° 50' N. 02° 0 6 ' E).
performed.
T h e climate is o c e a n i c with continental influence, the
m e a n annual rainfall is 6 0 6 mm and the m e a n annual
* M u s é u m National d ' H i s t o i r e Naturelle. É q u i p e P a r a s i t o l o g i e c o m p a r é e et m o d è l e s
e x p é r i m e n t a u x a s s o c i é e à l'INSERM,
U567
et
temperature
10.3° C. T h e terrain is mesophilic grass-
land.
L a b o r a t o i r e d e P r o t o z o o l o g i e et P a r a s i t o l o g i e c o m p a r é e ( E P H E ) , 6 1 ,
Donzère-Mondragon
rue B u f f o n . 7 5 2 3 1 Paris C e d e x 0 5 , F r a n c e .
south-east o f France (departments o f D r o m e and Vau-
C o r r e s p o n d e n c e : Irène Landau.
T e l . : + 3 3 (0)1 4 0
79
35 0 0 - Fax: +33 (0)1 4 0 7 9 3 4 9 9 .
E-mail: l a n d a u @ c i m r s 1 . m n h n . f r
Parasite. 2003. to. 5 1 - 5 7
reserve covers 1.545 ha in the
cluse, 4 4 ° 2 6 ' N, 4° 4 2 ' E). T h e climate is mediterran e a n with continental influence. T h e mean annual rain-
Mémoire
51
GRÈS V., VOZA T., CHABAUD A. & LANDA'
Caecal contents were diluted with two volumes o f 2.5 %
potassium dichromate solution and samples w e r e kept
for three days at room temperature o f 24° C, in large
Petri dishes to allow maturation o f the oocysts. T h e
faecal suspensions w e r e then filtered through sieves
o f decreasing mesh size ( 4 0 0 µm, 2 0 0 urn, 100 µm).
Oocysts were isolated by magnesium sulphate flotation,
identified and counted with the aid o f a MacMaster cell.
Results are expressed as the n u m b e r o f oocysts per
gram o f caecal contents. T h e age o f rabbits was evaluated by weighing the crystalline lenses, previously
fixed with formaldehyde solution. Rabbits w e r e classified as young (crystalline lenses weighing less than
100 mg) or adult (crystalline lenses weighing more than
100 m g ) according to Myers & Gilbert ( 1 9 6 8 ) .
Sporulated oocysts w e r e identified according to the
published morphological criteria, particularly those o f
Coudert et al. ( 1 9 9 5 ) .
fall is 8 6 0 m m and the m e a n annual temperature
12.8° C. It is very diversified xerophilic wasteland supporting Graminaceae, F a b a c e a e and Compositae and
s o m e shrubs, mainly Cornus sanguined,
Populus
alba.
P. nigra. Crataegus
monogyna
and Robinia
pseudacacia.
Massereau reserve covers 3 9 3 ha in the west o f France
(department o f Loire-Atlantique 4 7 ° 14' N, 0 1 ° 5 5 ' W ) .
The climate is o c e a n i c , the mean annual rainfall is
780 m m and the mean annual temperature 11.7°C. It
comprises mesophilic meadowland with mainly Agrostis sp., Oleus lanatus and Trifolium spp., a canal border
with Iris spp, Joncus
spp, Pbragmites
communis
and
a dam bordering a swamp, with Primus spinosa
and
Rubus
fructicosus.
Gerstheim reserve has an area o f 2,630 ha; it is located
in the east o f France (department o f Bas-Rhin) ( 4 8 °
22' N, 7 ° 4 2 ' E ) . T h e climate is continental, the mean
annual rainfall is 6 5 0 mm and the m e a n annual temp e r a t u r e is 1 0 ° C. T h e r e g i o n u s e d for t r a p p i n g
consisted o f three artificial sites with small shrubby
vegetation o f the m e s o b r o m e t u m or m e s o x e r o b r o metum type.
RESULTS
T
en species were identified: Eimeria
perforans
(Leuckart, 1879); E. f l a v e s c e n s Marotel & Guilhon,
194T, E. piriformis
Kotlan & P ô s p e s c h 1934;
E. exigua
Yakimoff, 1 9 3 4 ; E. media
Kessel, 1929;
E. magna
Pérard, 1925; E. intestinalis
Cheissin, 1948;
E. stiedai (Lindemann, 1865); E. coecicola
Cheissin,
1947 and E. roobroucki
described recently by Grès,
Marchandeau & Landau ( 2 0 0 2 ) . No specific hare c o c cidia w e r e identified.
Beniguet island reserve has an area o f 6 4 ha and is
located three miles off Conquet in Brittany ( 4 8 ° 2 1 ' N,
04° 5 1 ' W ) . T h e climate is o c e a n i c , the m e a n annual
rainfall is 8 0 0 m m and the m e a n annual temperature
is 1 1 . 8 ° C . T h e terrain c o m p r i s e s x e r o p h i l i c dunes
c o v e r e d with Armeria
maritima,
Festuca
rubra,
Senecio
jacobaea,
Silenae
matitima
and Carex
arenaria.
It was not possible to evaluate, in the various reserves,
the rabbits density per hectare.
Five rabbits w e r e usually caught each month from
February 1998 to February 1999 in the five mainland
areas.
Detailed figures o f prevalence and parasite load have
b e e n recorded in a b o o k (LV) deposited in our laboratory (Parasitologie comparée et modèles expérimentaux)
at the Muséum National d'Histoire Naturelle in Paris.
The sex o f the animals had n o impact on infections
which varied with the age o f the rabbits, the season
and the locality.
Twenty rabbits were caught on a single occasion in the
Beniguet reserve, on the 23 and 24th o f September 1998.
Tables I to IV and figures 1 to 4 summarize our results.
It was not possible to publish here all the detailed
SAMPLING
Arjuzanx
Béniguet
Chèvreloup
Donzère-M.
Massereau
Gerstheim
(n = 4 4 )
(n = 1 9 )
(n = 19)
(n = 5 3 )
(n = 3 9 )
(n = 4 3 )
E.
perforans
923 ± 545
228 ± 52
596 ± 123
2.069 ± 733
flavescens
276 ± 59
189 ± 7 3
221 ± 6 2
11.499 ± 5.449
E.
4,583 ± 2,246
327 ± 7 0
1,183
±
125 ± 7 2
270 ± 146
2 , 8 9 7 ± 1,423
193 ± 3 9
4 0 ± 14
733 ± 433
1,490
± 1.106
E.
media
E.
exigua
E.
piriformis
E.
stiedai
E.
magna
E.
coecicola
E.
intestinalis
E.
roobroucki
8 ± 2
70
± 20
10 ± 1 0
1 ± 0.3
3 ± 2
170 ± 1 3 8
7 ± 5
15 ± 7
17 ± 1 4
0.4 ±
0.4
0
38 ±
34
2
±
1
0.7 ± 0 . 4
1,937
±
1.121
5,596 ± 2,817
54
± 40
84 ± 65
665 ± 4 8 6
3,151
± 2,842
0
485
5 ± 3
3 9 ± 14
585 ± 544
67 ± 2 3 4
56 ± 20
77 ± 25
0.4
± 0.4
2 ± 1
11 ±
6
5 ±
4
6 ± 6
5 ± 3
In + 5
18 ±
15
0
0.1 ± 0.1
0.1 ± 0.1
2 ± 2
110 ±
54
13 ± 13
1 ± 1
T a b l e I. - M e a n parasitic l o a d of adult r a b b i t s a c c o r d i n g to locality ( ± s t a n d a r d d e v i a t i o n ) .
52
Parasite, 2003, 10. 51-57
EIMERIA O F W I L D R A B B F T S
Arjuzanx
Béniguet
Chèvreloup
Donzère-M.
Massereau
Gerstheim
(n = 9 )
(n = 1 )
(n = 9 )
(n = 7 )
( n = 1)
(n = 10)
E.
perforans
16.840 ± 7,415
164
167,545 ± 80,793
13,763 ± 10,370
4,453
107.236 ± 69,381
E.
flavescens
4,529 ± 2.390
15
3 , 0 2 1 ± 1.269
4,593
0
43,372 ± 41,738
E.
media
19,935 ± 13,566
0
76,533 ± 43,807
19.885 ± 16.689
E.
exigua
874 ± 652
0
1.988 ± 1,196
140
11,121 ± 6,399
285 ± 179
234 ± 106
72.112 ± 50,966
E.
piriformis
4 ± 4
1 , 3 5 0 ± 1,071
0
49,923 ± 28,414
2,512 ± 2.139
0
14.025 ± 12,621
73
347
45,768 ± 27,327
E.
stiedai
9,575 ± 9,408
E.
magna
1,785 ± 1.566
6
52,014 ± 51,483
975 ± 780
120
20.995 ± 13,265
38 ± 38
0
38,941 ± 25,536
193
0
32.933 ± 16.055
0
0
0
0
E.
coecicola
E.
intestinalis
0
0
16,732 ± 10,810
53 ± 53
0
E.
roobroucki
0
0
0
0
T a b l e II. - M e a n parasitic l o a d o f j u v e n i l e r a b b i t s , a c c o r d i n g t o locality ( ± s t a n d a r d d e v i a t i o n ) .
Spring ( n = 5 2 )
E.
perforans
783 ± 1 8 9
E.
flavescens
2 9 3 ± 48
E.
media
E.
exigua
E.
piriformis
Summer ( n = 4 0 )
A u t u m n (n = 6 7 )
Winter ( n = 5 8 )
493 ± 230
1.109 ± 5 3 4
4 , 3 4 9 ± 1.890
1.333 ± 9 8 6
775 ± 267
979 ± 436
139 ± 97
603 ± 301
526 ± 323
2 6 ± 14
417 ± 353
1,50.3 ± 8 8 9
562 ± 377
249 ± 183
609 ± 369
1,132 ± 8 8 0
19 ± 15
10 ± 4
48 ± 19
102 ± 3 7
E.
stiedai
1 ± 0.6
E.
magna
5 ± 3
19 ± 13
2 ± 1
5 ± 5
28 ± 22
E.
coecicola
2 2 ± 13
70 ± 40
46 ± 37
E.
intestinalis
0
0
106 ± 8 4
213 ± 159
932 ± 932
E.
roobroucki
3 ± 2
0
0.2 ± 0.1
0.4 ± 0.2
T a b l e III. - M e a n parasitic l o a d o f adult r a b b i t s a c c o r d i n g t o s e a s o n ( ± s t a n d a r d d e v i a t i o n ) .
Spring ( n = 9 )
Summer ( n = 1 8 )
Autumn ( n = 9 )
133.554 ± 85,980
E.
perforans
68,597 ± 27,730
56,2.32 ± 3 7 , 7 3 8
E.
flavescens
11,118 ± 8.026
57.250 ± 45,502
3 , 2 3 9 ± 1.906
39,447 ± 23,868
E.
media
52,333 ± 44,422
50.211 ± 28,617
E.
exigua
4,124 ± 2,449
448 ± 332
833 ± 579
1,796 ± 1,726
4,075 ± 3,368
1,353 ± 6 5 8
92,789 ± 51.533
8.628 ± 8,224
4.983 ± 4,698
34,442 ± 26,120
40.518 ± 25,431
E.
piriformis
E.
stiedai
E.
magna
E.
coecicola
0
18,120 ± 9,407
385 ± 196
39,532 ± 25,744
E.
intestinalis
0
5.035 ± 5,035
6,663 ± 5,677
E.
roobroucki
0
0
0
T a b l e IV. - M e a n p a r a s i t i c l o a d o f j u v e n i l e r a b b i t s a c c o r d i n g t o s e a s o n ( ± s t a n d a r d d e v i a t i o n ) .
tables and graphs. T h e y may h o w e v e r b e found
in
INTENSITY O F INFECTION
V. Grès thesis ( 2 0 0 1 ) :
i) the m e a n parasite load o f adult ( T a b l e I) and young
Parasite load w a s variable in young rabbits, possibly
( T a b l e II) rabbits from e a c h locality (for all s e a s o n s
depending o n the uncertain c h a n c e o f their b e c o m i n g
together);
infected.
ii) the m e a n parasite load o f adult ( T a b l e III) and
In adult rabbits, intensity o f infection was generally
young ( T a b l e IV) rabbits at different seasons;
highest in winter. In young animals it was higher in
iii) prevalences o f the different s p e c i e s in e a c h study
spring and autumn than in s u m m e r e x c e p t for E. piri-
area throughout the year, in adult (Fig. 1) and young
formis
(Fig. 2) rabbits; and
In adult rabbits, the intensity o f infection was g e n e -
and E.
magna.
iv) prevalences o f the different species in adult (Fig. 3 )
rally highest in winter.
and young (Fig. 4 ) rabbits according to the season.
T h e principal feature determining the intensity of infec-
T h e r e w e r e no young rabbits present in winter.
tion was the geographical location. Parasite load was
Parasite, 2 0 0 3 . 10. 5 1 - 5 7
Mémoire
53
GRÈS V., VOZA T., CHABAUD A. & LANDAU I.
Fig. 1. - P r e v a l e n c e s o f t h e Eimeria
s p e c i e s in adult rabbits, a c c o r d i n g to locality.
Fig. 2. - P r e v a l e n c e s of t h e Eimeria
s p e c i e s in j u v e n i l e rabbits, a c c o r d i n g to locality.
54
Mémoire
Parasite, 2 0 0 3 , 10, 5 1 - 5 7
EIMERIA O F W I L D R A B B I T S
Fig. 3. - P r e v a l e n c e s of Eimeria
s p e c i e s in adult rabbits, a c c o r d i n g to s e a s o n .
Fig. 4. - P r e v a l e n c e s of Eimeria
s p e c i e s in j u v e n i l e rabbits, a c c o r d i n g to s e a s o n .
Parasite. 200.3. 10. 5 1 - 5 7
Mémoire
55
ORES V., VOZA T., CHABAUD A. & LANDAU I.
high in the humid and relatively cold localities (Ile de
France and Alsace), lower along the Atlantic littoral
(Loire and Landes) and lower still in the dryer and warmer areas ( R h o n e valley).
PREVALENCES
In adult rabbits, prevalence was highest with two species, E. perforans
and E. flavescens; it was moderately
high with E. media and E. piriformis,
and generally low
with the six other species.
Results from young rabbits were available (Figs 2 and
4 ) from only four locations (seven to 10 rabbits e x a mined from e a c h ) : Arjuzanx, Chevreloup, DonzèreMondragon and Gershteim. E. roobrouki
was absent
and E. intestinalis
was found only in Chevreloup.
Prevalences were, with few exceptions, remarkably
similar in the different localities: nearly 100 % with
E. perforans
and E. flavescens
and 7 0 % with the six
other s p e c i e s . T w o e x c e p t i o n s w e r e E.
piriformis,
absent from Gerstheim, and E. exigua and E.
coecicola,
which had low prevalences (around 10-30 % ) in Arjuzanx and Donzère-Mondragon.
The histogram o f prevalence (Fig. 4) according to season
shows least variability in autumn compared with spring
and summer, i.e. E. perforans
and E. flavescens
around
100 % and the six other species around 7 0 %.
With the adult rabbits, in contrast with the variability
o f parasite load according to location (Fig. 1), w e
observed stable prevalences: E. perforans
and E. flavescens, 9 0 - 1 0 0 %; E. piriformis,
70-95 %; E.
exigua,
32-72 %; E. media.
29-69 %; E. magna,
17-42 %;
E. coecicola.
5-32 %; E. stiedai, 4-21 %; E.
roobrouck,
0-21 %; and E. intestinalis,
0-16 %. Even more striking,
in all localities, the ranked order o f prevalence o f each
species was remarkably stable: E. perforans
and E. flavescens, 1-2; E. piriformis,
3; E. exigua, 4-5 (with lowparasite loads); E. media, 4-5; E. magna.
6;
coecicola and E. stiediai,
7-9; E. roobroucki
and E. intestinalis. 9 - 1 0 .
DISCUSSION
AND DOMESTIC RABBITS
or this type o f study, precise specific identification is necessary but the systematics o f Coccidia
are difficult. C o n g e n e r i c s p e c i e s are frequent
with the Nematodes, for example, and their morphology is varied with many differential characters, while
with Eimeria the morphology o f the oocyst, which is
the main criterion is a w e a k character. Confusion betw e e n species is always possible and it is disturbing to
find in the literature different biological characters
56
In contrast to these observations, in the wild rabbit in
its natural environment, in south-west Australia, H o b b s
& Twigg ( 1 9 9 8 ) found prevalences to b e very similar
to ours in France: E. perforans,
8 4 %; E.
flavescens,
60 %; E. piriformis,
50 %; E. exigua,
62 %; E.
media,
45 %; E. magna,
33 %; E. coecicola,
7 %; E. stiedai,
26 %; and E. intestinalis,
19 %. T h e only important difference was the p r e s e n c e in Australia of E.
irresidua
(9 % ) and the a b s e n c e o f E. roobroucki.
This was not
true, however, for the parasite intensities.
THE
COMPARISON O F COCCIDIOSIS O F WILD
F
assigned to the same species by reliable authors. In
the same way the origin o f strains is not always specified, and biological differences observed amongst
strains may in fact represent subspeciation.
The parasitism o f domestic rabbits differs from that in
the wild: Zundel ( 1 9 7 9 ) carried out a survey in breeding colonies in different parts o f France and listed
nine intestinal species. T w o o f the species recorded,
although designated by different names, correspond to
species found by us in the wild: Eimeria
sp. sensu
Zundel = E. flavescens. and E. neoleporis
sensu Zundel = E. coecicola.
His list differs from ours by the pres e n c e o f E. irresidua and the a b s e n c e o f E. exigua and
E. roobroucki.
T h e percentages o f prevalence ( P ) and
parasite load (PL) w e r e approximately as follows:
E. perforans:
P 8 7 % , PL 37 %; E. media: P 55 %,
PL 10 %; E. magna:
P 53 %, PL 37 %;
flavescens:
P 30 %, PL 1 %; E. irresidua:
P 25 % , PL 1 %; E. intestinalis-. P 21 %, PL 10 %; E. piriformis:
P 13 %, PL 1 %;
and E. coecicola:
P 11 %, PL 10 %. However, contraty
to what w e observed with wild rabbits, the ranking o f
prevalence varied from o n e region to the other.
T h e predominance in breeding colonies of domestic
rabbits o f the three species E. perforans,
E. media and
E. magna
has also b e e n reported in Italy (Gallazzi,
1977), England (Catchpole & Norton, 1979), Belgium
(Peeters & G e e r o m s , 1981), Saudi Arabia (Kasim & AlShawa, 1 9 8 7 ) , Nigeria ( O k e w o l e , 1 9 9 0 ) , and India
(Souza et al., 1993). T h e s e species remained dominant
in the industrial breeding colonies after developing
resistance to robenidine.
BALANCE BETWEEN CONGENERIC SPECIES
Several factors have influenced speciation o f
Eimeria
in rabbits: a long evolutionary period, the Lagomorpha
having evolved little since the E o c e n e and having
retained their parasitic fauna, and geographical isolation together with m o n o x e n o u s life cycles and oocysts
which appear to b e (Coudert & Ivoré, 1973) fragile and
destroyed by heat.
Rabbits are strictly herbivorous, but they are opportunistic feeders which accounts for the variability o f
parasite intensity from e a c h individual. H o w e v e r the
stability o f the rank o f prevalence indicates an ancient
and highly stable equilibrium.
Mémoire
Parasite, 2 0 0 3 , 10, 5 1 - 5 7
EìMERIA O F W I L D
ACKNOWLEDGEMENTS
RABBITS
E. Coccidies et coccidioses intestinales du lapin - étude
bibliographique, enquête épidémiologique. Veterinary thesis, Créteil University, 1 9 7 9 .
ZUNDEL
T
his study was supported by a grant from the
Office National de la Chasse et de la Faune Sauvage (ONCFS). W e are very grateful to F. Biady,
director o f CNERA for allowing our work to b e carried out in the national reserves o f ONCFS and to the
colleagues w h o collected the biological material, particularly S. Avignon, G. Delacour, J.C. Gauclin, F. Bernard and G. Leray. W e are m u c h indebted to A. R o o brouck for his help in the work performed at Versailles
and to S. Marchandeau for his constant help and
advice throughout this study. Many thanks to J o h n
Baker and Jean-Charles Gantier for their great help.
Reçu le 13 juillet 2 0 0 2
Accepté le 1 2 décembre 2 0 0 2
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